Stingless Bee, Trigona Spinipes James C

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Stingless Bee, Trigona Spinipes James C Received 13 November 2003 Accepted 11 February 2004 Published online 15 June 2004 Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes James C. Nieh1*, Lillian S. Barreto2, Felipe A. L. Contrera3 and Vera L. Imperatriz-Fonseca3 1University of California San Diego, Division of Biological Sciences, Section of Ecology, Behavior and Evolution, Mail Code 0116, La Jolla, CA 92093, USA 2Empresa Baiana de Desenvolvimento Agricola, Laboratorio de Abelhas (LABE), Avenue Ademar de Barros N 967, Salvador-Bahia, Brazil 3Instituto de Biocieˆncias, Laborato´rio de Abelhas, Universidade de Sa˜o Paulo, Sa˜o Paulo 05508-900, SP, Brazil Signals that are perceived over long distances or leave extended spatial traces are subject to eavesdropping. Eavesdropping has therefore acted as a selective pressure in the evolution of diverse animal communication systems, perhaps even in the evolution of functionally referential communication. Early work suggested that some species of stingless bees (Hymenoptera, Apidae, Meliponini) may use interceptive olfactory eavesdropping to discover food sources being exploited by competitors, but it is not clear if any stingless bee can be attracted to the odour marks deposited by an interspecific competitor. We show that foragers of the aggressive meliponine bee, Trigona spinipes, can detect and orient towards odour marks deposited by a competitor, Melipona rufiventris, and then rapidly take over the food source, driving away or killing their competitors. When searching for food sources at new locations that they are not already exploiting, T. spinipes foragers strongly prefer M. rufiventris odour marks to odour marks deposited by their own nest- mates, whereas they prefer nest-mate odour marks over M. rufiventris odour marks at a location already occupied by T. spinipes nest-mates. Melipona rufiventris foragers flee from T. spinipes odour marks. This olfactory eavesdropping may have played a role in the evolution of potentially cryptic communication mechanisms such as shortened odour trails, point-source only odour marking and functionally referential communication concealed at the nest. Keywords: eavesdropping; olfaction; competition; aggression; evolution of communication 1. INTRODUCTION (Nieh 1999). Several species of stingless bees use extended odour trails to communicate food location (Kerr 1960). Eavesdropping plays a significant role in the evolution of Recently, an intermediate strategy was described for a complex and sophisticated communication networks in stingless bee, Trigona hyalinata, which uses a short odour animals ranging from songbirds to fishes (McGregor trail extending only a short distance from the food source 1993; Stowe et al. 1995; Oliveira et al. 1998; Peake et al. towards the nest (Nieh et al. 2003a). Other meliponine 2002; Whitfield 2002) and may play a role in shaping bee species, including those that may use functionally referen- communication (Nieh 1999). Signals that are sent over tial communication, do not use odour trails and odour long distances or leave extended spatial traces are suscep- mark the food source alone (Nieh & Roubik 1995; Hrncir tible to eavesdropping (McGregor 1993), and thus some et al. 2000; Nieh et al. 2003c). Intriguingly, honeybees extirpating stingless bee species (Hymenoptera, Apidae, odour mark only the food source and use functionally ref- Meliponini) are hypothesized to use interceptive olfactory erential communication, encoding food location through eavesdropping (intercepting signals intended for other a waggle dance at the nest (Esch et al. 2001; Dyer 2002). receivers (Peake 2004)) to detect valuable food sources Stingless bees are all highly social (Michener 2000), discovered by other bees (Kerr et al. 1963), whereas other occupy environments where food resources are seasonally species may detect the pheromones of aggressive melipon- scarce and can be highly sought after, and recruit nest- ine species to avoid costly conflicts with superior competi- mates to these resources (Johnson 1974; Roubik 1982; tors (Johnson 1974; Hubbell & Johnson 1978). Eltz et al. 2001, 2002; Liow et al. 2001). To help guide Such olfactory eavesdropping could have contributed to nest-mates during recruitment, certain species deposit the evolution of concealed communication inside the nest odour trails beginning near the nest and extending to the (Nieh 1999), and thus to the evolution of functionally ref- food source (Lindauer & Kerr 1958). Kerr (1960) reports erential communication (the ability to abstractly encode a T. amalthea odour trail extending for 900 m, and the environmental information into signals understood by foraging ranges of many meliponine species are thought receivers (Marler et al. 1992; Blumstein 1999)) as referen- to extend for at least several hundred metres (Roubik & tial location information replaced odour trail information Aluja 1983; Van Nieuwstadt & Ruano 1996). Such odour trails would create a long but relatively narrow active space and could be detected by scout bees whose search paths intersected the active space, with the probability of inter- * Author for correspondence ([email protected]). section increasing with trail length. The cross-sectional Proc. R. Soc. Lond. B (2004) 271, 1633–1640 1633 2004 The Royal Society DOI 10.1098/rspb.2004.2717 1634 J. C. Nieh and others Olfactory eavesdropping by Trigona spinipes active space of meliponine odour trails has not been s1 measured, although odours deposited at a feeder by 100 m Melipona panamica foragers can attract nest-mates over distances of 6 to 12 m (Nieh 1998). It is not known if interspecific meliponine eavesdrop- ping actually occurs. Kerr et al. (1963) suggested that r2 fr2 Scaptotrigona xanthotricha may orient towards S. postica r1 fr1 odour marks. They trained colonies of S. postica and S. xanthotricha to separate feeders placed such that the odour trails from both colonies crossed. Two out of 122 S. postica foragers arrived at the S. xanthotricha feeder, fs whereas 28 out of 124 S. xanthotricha foragers arrived at s2 the S. postica feeder. These results are suggestive, but it is unclear how many foragers would have arrived at the Figure 1. Research site plan. Squares indicate colonies. Open circles indicate feeder sites. Lines connect colonies to feeder of the other species in the absence of odour marks. the feeder sites used with each colony. The star denotes the Sensitivity to interspecific odour marks may also work to global positioning system reference point: 21°26.387Ј S, the advantage of the excluded, allowing frequently 47°34.884Ј W. attacked species to detect aggressive species before serious attacks begin. Johnson (1974) noted that T. fulviventris 2. MATERIAL AND METHODS foragers appeared reluctant to land on food sites pre- viously visited by the aggressive species, T. fuscipennis (a) Study site, feeders and training (Johnson & Hubbell 1974). However, it is not clear if any We used two colonies of T. spinipes (s1 and s2, ca. 8000 bees stingless bee can be attracted to or repulsed by the per colony) in trees and two colonies of M. rufiventris (r1 and food-marking odours deposited by an interspecific r2, 500–700 bees per colony) in hives at a ranch near Sa˜o Sima˜o competitor. in the state of Sa˜o Paulo, Brazil, from August to September in We therefore chose to study the highly aggressive spec- 2002 and 2003. We studied the following pairs of colonies: 1 (s ,r); 1 (s ,r); 2 (s ,r); and 2 (s ,r) for a total of six trials ies T. spinipes, which defends and usurps food sources 1 1 1 2 2 1 2 2 from carpenter bees, Africanized honeybees and other per experiment. stingless bees (Cobert & Willmer 1980; Cortopassi-Laur- We trained 20 individually marked foragers from each M. rufi- ventris colony to feeders located 2 m east of each colony (f ) ino 1982; Cortopassi-Laurino & Ramalho 1988; Gallo et r (figure 1). We then trained 20 individually marked foragers from al. 1988; Sazima & Sazima 1989; Martinez & Bullock each T. spinipes colony to identical feeders located 4 m east of 1990; Ramalho et al. 1994; Silva et al. 1997), six species each M. rufiventris colony (f ). After one trial at f and one trial of passiform birds (Barbosa 1999) and several species of s s at f , we captured and removed all T. spinipes and M. rufiventris hummingbirds (Willmer & Corbet 1981; Gill et al. 1982). r foragers that had been trained to the feeders, and then trained Trigona spinipes foragers use cephalic glandular sections to a new group of foragers from each colony. We verified that all deposit odour trails and to odour-mark food sources (Kerr trained foragers came from the pair of colonies under study by 1972, 1973; Kerr et al. 1981). watching them enter their respective colony entrances. With Trigona spinipes is a foraging generalist (Barbola et al. each T. spinipes colony, we used aspirators (Nieh 1998) to cap- 2000) and inhabits diverse habitats, ranging from the cer- ture all foragers at the feeders and verifying for 3 h that no rado (neotropical savannah) to tropical forests throughout further foragers arrived at any feeder location before training for- South America (Schwarz 1948; Roubik 1989; Barros Hen- agers from the second colony. With M. rufiventris, we used wire riques 1997). Throughout its range, T. spinipes constructs mesh (applied in the evening after all bees had returned to their large external nests of mud, resin and wax, usually placed nest) to seal the entrance to the colony that was not under study. above the ground in large trees (Roubik 1989). Colonies Each feeder consisted of a small glass bottle (5 cm diameter, range in size from 5000 to over 100 000 workers 4.5 cm high, 65 ml) inverted over a grooved plastic base 6.7 cm (Michener 1974; Wille 1983; Almeida & Laroca 1988), in diameter (methods of Von Frisch 1967). To facilitate forager and thus T. spinipes form some of the largest stingless bee orientation, we placed a disc of yellow paper 6.7 cm in diameter colonies in the world (Roubik 1989).
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